Sperm chromatin condensation: epigenetic mechanisms to compact the genome and spatiotemporal regulation from inside and outside the nucleus

Okada, Yuki

doi:10.1266/ggs.21-00065

Cited by 20 publications

(10 citation statements)

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“…In most animals, chromatin is required to rely on special sperm nuclear basic protein to reconstitute into a more compact form for spermatogenesis(Torok and Gornik 2018; Kimura and Loppin 2016). Generally, most of the core histones will be replaced by protamine rich in lysine and cysteine residues, thereby packaging the sperm genome into a unique circular chromatin structure, which is conducive to protecting the genetic material from mechanical damage, oxidative damage, bacterial infection, and so on (Hao et al 2019;Okada 2022). Thus, as spermatogenesis goes forward, there is a steady decrease in histones and, in turn, a corresponding decrease in the enzymes involved in histone modi cations.…”

Section: Discussionmentioning

confidence: 99%

HAT1 participates in spermatogenesis of Eriocheir sinensis by regulating chromatin aggregation

Liu

Tang

Sun

et al. 2023

Preprint

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Chinese mitten crab, Eriocheir sinensis, is a decapod crustacean with a special, non-condensated nucleus in the sperm. Studies has shown that this is closely related to histone modification. To explore the possible role of histone acetyltransferase 1 (HAT1) in the non-condensation mechanism of sperm nucleus and the spermatogenesis of E. sinensis, we took the testis tissues of adult and juvenile crabs as the objects of study and analyzed their biological functions by whole transcriptome sequencing and bioinformatics, then further analyzed the expression and distribution of HAT1 through RT-qRCR, western blotting, and immunofluorescence. The results showed that HAT1 was up-regulated in adult testes compared with in the juvenile ones (n = 3, P < 0.05). Besides, HAT1 was mainly located in the nucleus of the male germ cell of E. sinensis. With the development of spermatogonia, the expression of HAT1 decreased (n = 3, P < 0.05), and the sperm nucleus of E. sinensis also gradually become non-condensed. Bioinformatics analysis shows that HAT1 and proteins such as Asf1b, Chaf1b and Hist1h3f are involved in biological processes such as DNA conformational changes and DNA replication-dependent nucleosome assembly. It follows that HAT1 is an important regulator of maintaining histone acetylation at specific levels. During the spermatogenesis of E. sinensis, HAT1 first loosens the chromatin structure of sperm nucleus by acetylating histone, while the reduction of HAT1 expression in the later stage effectively avoids excessive acetylation, and maintains histone acetylation at a specific level, which protects the nuclear chromatin state of non-condensed sperm and is important in the spermatogenesis of E. sinensis.

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Section: Discussionmentioning

confidence: 99%

HAT1 participates in spermatogenesis of Eriocheir sinensis by regulating chromatin aggregation

Liu

Tang

Sun

et al. 2023

Preprint

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“…The data from this study showed that mRNA and protein IGF2 are expressed in human spermatozoa, suggesting that the IGF2 gene is both transcribed and translated. This is more likely to happen in spermatogonia or spermatocytes, during the early phases of spermatogenesis, due to the highly degree of chromatin compactness in spermatozoa ( 57 ). However, the possibility that these processes may even partially occur in spermatozoa cannot be completely ruled out as some regions of the sperm genome are accessible to the transcriptional machinery ( 58 ).…”

Section: Discussionmentioning

confidence: 99%

Sperm-carried IGF2 downregulated the expression of mitogens produced by Sertoli cells: A paracrine mechanism for regulating spermatogenesis?

et al. 2022

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IntroductionInsulin-like growth factor 2 (IGF2) mRNA has been found in human and mouse spermatozoa. It is currently unknown whether the IGF2 protein is expressed in human spermatozoa and, if so, its possible role in the cross-talk between germ and Sertoli cells (SCs) during spermatogenesis.MethodsTo accomplish this, we analyzed sperm samples from four consecutive Caucasian men. Furthermore, to understand its role during the spermatogenetic process, porcine SCs were incubated with increasing concentrations (0.33, 3.33, and 10 ng/mL) of recombinant human IGF2 (rhIGF2) for 48 hours. Subsequently, the experiments were repeated by pre-incubating SCs with the non-competitive insulin-like growth factor 1 receptor (IGF1R) inhibitor NVP-AEW541. The following outcomes were evaluated: 1) Gene expression of the glial cell-line derived neurotrophic factor (GDNF), fibroblast growth factor 2 (FGF2), and stem cell factor (SCF) mitogens; 2) gene and protein expression of follicle-stimulating hormone receptor (FSHR), anti-Müllerian hormone (AMH), and inhibin B; 3) SC proliferation.ResultsWe found that the IGF2 protein was present in each of the sperm samples. IGF2 appeared as a cytoplasmic protein localized in the equatorial and post-acrosomal segment and with a varying degree of expression in each cell. In SCs, IGF2 significantly downregulated GDNF gene expression in a concentration-dependent manner. FGF2 and SCF were downregulated only by the highest concentration of IGF2. Similarly, IGF2 downregulated the FSHR gene and FSHR, AMH, and inhibin B protein expression. Finally, IGF2 significantly suppressed the SC proliferation rate. All these findings were reversed by pre-incubation with NVP-AEW541, suggesting an effect mediated by the interaction of IGF2 with the IGFR.ConclusionIn conclusion, sperm IGF2 seems to downregulate the expression of mitogens, which are known to be physiologically released by the SCs to promote gonocyte proliferation and spermatogonial fate adoption. These findings suggest the presence of paracrine regulatory mechanisms acting on the seminiferous epithelium during spermatogenesis, by which germ cells can influence the amount of mitogens released by the SCs, their sensitivity to FSH, and their rate of proliferation.

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“…Second, some sperm‐borne organelles introduced into the oocyte, such as mitochondria, are degraded by specific mechanisms 7,8 . Finally, prior to fertilization, the oocyte arrests in a quiescent state with extremely depressed transcriptional and translational activity, 9–11 while the spermatozoa replace histones, which provides structural support to the chromosome, with protamine to reduce chromosomal volume, consequently losing transcriptional or translational activity 12,13 . These facts indicate that de novo protein synthesis is severely depressed during terminal differentiation of mammalian gametes and immediately after fertilization, strongly suggesting that the content, interactions, enzymatic activities, and dynamics of oocyte components significantly determine embryonic quality.…”

Section: Introductionmentioning

confidence: 99%

“…7,8 Finally, prior to fertilization, the oocyte arrests in a quiescent state with extremely depressed transcriptional and translational activity, [9][10][11] while the spermatozoa replace histones, which provides structural support to the chromosome, with protamine to reduce chromosomal volume, consequently losing transcriptional or translational activity. 12,13 These facts indicate that de novo protein synthesis is severely depressed during terminal differentiation of mammalian gametes and immediately after fertilization, strongly suggesting that the content, interactions, enzymatic activities, and dynamics of oocyte components significantly determine embryonic quality. Importantly, maternal organelles that play essential roles in various cellular functions, increase quantitatively during follicular development and changes qualitatively during oocyte maturation, indicated by localization and activities (Figure 1).…”

mentioning

confidence: 99%

Reorganization, specialization, and degradation of oocyte maternal components for early development

Satouh

Sato

2023

Reprod Medicine & Biology

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Background Oocyte components are maternally provided, solely determine oocyte quality, and coordinately determine embryo quality with zygotic gene expression. During oocyte maturation, maternal organelles are drastically reorganized and specialized to support oocyte characteristics. A large number of maternal components are actively degraded after fertilization and gradually replaced by zygotic gene products. The molecular basis and the significance of these processes on oocyte/embryo quality are not fully understood. Methods Firstly, recent findings in organelle characteristics of other cells or oocytes from model organisms are introduced for further understanding of oocyte organelle reorganization/specialization. Secondly, recent progress in studies on maternal components degradation and their molecular mechanisms are introduced. Finally, future applications of these advancements for predicting mammalian oocyte/embryo quality are discussed. Main findings The significance of cellular surface protein degradation via endocytosis for embryonic development, and involvement of biogenesis of lipid droplets in embryonic quality, were recently reported using mammalian model organisms. Conclusion Identifying key oocyte component characteristics and understanding their dynamics may lead to new applications in oocyte/embryo quality prediction and improvement. To implement these multidimensional concepts, development of new technical approaches that allow us to address the complexity and efficient studies using model organisms are required.

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Sperm chromatin condensation: epigenetic mechanisms to compact the genome and spatiotemporal regulation from inside and outside the nucleus

Cited by 20 publications

References 152 publications

HAT1 participates in spermatogenesis of Eriocheir sinensis by regulating chromatin aggregation

HAT1 participates in spermatogenesis of Eriocheir sinensis by regulating chromatin aggregation

Sperm-carried IGF2 downregulated the expression of mitogens produced by Sertoli cells: A paracrine mechanism for regulating spermatogenesis?

Reorganization, specialization, and degradation of oocyte maternal components for early development

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